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Significance

Bacteria and archaea have small genomes with tightly packed protein-coding genes. Typically, this genome architecture is explained by “genome streamlining” (minimization) under selection for high replication rate. We developed a mathematical model of microbial evolution and tested it against extensive data from multiple genome comparisons to identify the key evolutionary forces. The results indicate that genome evolution is not governed by streamlining but rather, reflects the balance between the benefit of additional genes that diminishes with the genome size and the intrinsic preference for DNA deletion over acquisition. These results explain the observation that, in an apparent contradiction with the population genetic theory, microbes with large genomes reach higher abundance and are subject to stronger selection than small “streamlined” genomes.

Abstract

Bacteria and archaea typically possess small genomes that are tightly packed with protein-coding genes. The compactness of prokaryotic genomes is commonly perceived as evidence of adaptive genome streamlining caused by strong purifying selection in large microbial populations. In such populations, even the small cost incurred by nonfunctional DNA because of extra energy and time expenditure is thought to be sufficient for this extra genetic material to be eliminated by selection. However, contrary to the predictions of this model, there exists a consistent, positive correlation between the strength of selection at the protein sequence level, measured as the ratio of nonsynonymous to synonymous substitution rates, and microbial genome size. Here, by fitting the genome size distributions in multiple groups of prokaryotes to predictions of mathematical models of population evolution, we show that only models in which acquisition of additional genes is, on average, slightly beneficial yield a good fit to genomic data. These results suggest that the number of genes in prokaryotic genomes reflects the equilibrium between the benefit of additional genes that diminishes as the genome grows and deletion bias (i.e., the rate of deletion of genetic material being slightly greater than the rate of acquisition). Thus, new genes acquired by microbial genomes, on average, appear to be adaptive. The tight spacing of protein-coding genes likely results from a combination of the deletion bias and purifying selection that efficiently eliminates nonfunctional, noncoding sequences.

Significance

Bacteria and archaea have small genomes with tightly packed protein-coding genes. Typically, this genome architecture is explained by “genome streamlining” (minimization) under selection for high replication rate. We developed a mathematical model of microbial evolution and tested it against extensive data from multiple genome comparisons to identify the key evolutionary forces. The results indicate that genome evolution is not governed by streamlining but rather, reflects the balance between the benefit of additional genes that diminishes with the genome size and the intrinsic preference for DNA deletion over acquisition. These results explain the observation that, in an apparent contradiction with the population genetic theory, microbes with large genomes reach higher abundance and are subject to stronger selection than small “streamlined” genomes.

Abstract

Bacteria and archaea typically possess small genomes that are tightly packed with protein-coding genes. The compactness of prokaryotic genomes is commonly perceived as evidence of adaptive genome streamlining caused by strong purifying selection in large microbial populations. In such populations, even the small cost incurred by nonfunctional DNA because of extra energy and time expenditure is thought to be sufficient for this extra genetic material to be eliminated by selection. However, contrary to the predictions of this model, there exists a consistent, positive correlation between the strength of selection at the protein sequence level, measured as the ratio of nonsynonymous to synonymous substitution rates, and microbial genome size. Here, by fitting the genome size distributions in multiple groups of prokaryotes to predictions of mathematical models of population evolution, we show that only models in which acquisition of additional genes is, on average, slightly beneficial yield a good fit to genomic data. These results suggest that the number of genes in prokaryotic genomes reflects the equilibrium between the benefit of additional genes that diminishes as the genome grows and deletion bias (i.e., the rate of deletion of genetic material being slightly greater than the rate of acquisition). Thus, new genes acquired by microbial genomes, on average, appear to be adaptive. The tight spacing of protein-coding genes likely results from a combination of the deletion bias and purifying selection that efficiently eliminates nonfunctional, noncoding sequences.

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